Developmental control of a parAB promoter leads to formation of sporulation-associated ParB complexes in Streptomyces coelicolor

Journal of Bacteriology

Volumn 188, Issue 5, 2006, Pages 1710-1720

  Jakimowicz, Dagmara ^a,b   Mouz, Sebastien ^a,c   Zakrzewska Czerwińska, Jolanta ^b   Chater, Keith F ^a  

^a JOHN INNES CENTRE   (United Kingdom)

^b INSTITUTE OF IMMUNOLOGY AND EXPERIMENTAL THERAPY   (Poland)

^c Protein'Expert SA   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; GREEN FLUORESCENT PROTEIN; PARB PROTEIN; UNCLASSIFIED DRUG;

BACTERIAL CHROMOSOME; BACTERIAL GENE; BACTERIAL GROWTH; CELL STRUCTURE; CHROMOSOME SEGREGATION; COMPLEX FORMATION; CONFERENCE PAPER; CONTROLLED STUDY; FTSZ GENE; GENE EXPRESSION; GENE MUTATION; LIFE CYCLE; NONHUMAN; PARAB GENE; PARS GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; REGULATOR GENE; SPOROGENESIS; STREPTOMYCES COELICOLOR; TRANSCRIPTION REGULATION; WHIA GENE; WHIB GENE; WHIH GENE; WHII GENE;

BACTERIAL PROTEINS; CHROMOSOMES, BACTERIAL; ENDODEOXYRIBONUCLEASES; GENE EXPRESSION REGULATION, BACTERIAL; OPERON; PROMOTER REGIONS (GENETICS); SPORES, BACTERIAL; STREPTOMYCES COELICOLOR; TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS); STREPTOMYCES COELICOLOR;

EID: 33644786320     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.188.5.1710-1720.2006     Document Type: Conference Paper

References (52)

1. Ainsa, J. A., H. D. Parry, and K. F. Chater. 1999. A response regulator-like protein that functions at an intermediate stage of sporulation in Streptomyces coelicolor A3(2). Mol. Microbiol. 34:607-619.
2. Ainsa, J. A., N. J. Ryding, N. Hartley, K. C. Findlay, C. J. Bruton, and K. F. Chater. 2000. WhiA, a protein of unknown function conserved among gram-positive bacteria, is essential for sporulation in Streptomyces coelicolor A3(2). J. Bacteriol. 182:5470-5478.
3. Bartosik, A. A., and G. Jagura-Burdzy. 2005. Bacterial chromosome segregation. Acta Biochim. Pol. 52:1-34.
4. Bartosik, A. A., K. Lasocki, J. Mierzejewska, C. M. Thomas, and G. Jagura-Burdzy. 2004. ParB of Pseudomonas aeruginosa: interactions with its partner ParA and its target parS and specific effects on bacterial growth. J. Bacteriol. 186:6983-6998.
5. Bentley, S. D., K. F. Chater, A. M. Cerdeno-Tarraga, G. L. Challis, N. R. Thomson, K. D. James, D. E. Harris, M. A. Quail, H. Kieser, D. Harper, A. Bateman, S. Brown, G. Chandra, C. W. Chen, M. Collins, A. Cronin, A. Fraser, A. Goble, J. Hidalgo, T. Hornsby, S. Howarth, C. H. Huang, T. Kieser, L. Larke, L. Murphy, K. Oliver, S. O'Neil, E. Rabbinowitsch, M. A. Rajandream, K. Rutherford, S. Rutter, K. Seeger, D. Saunders, S. Sharp, R. Squares, S. Squares, K. Taylor, T. Warren, A. Wietzorrek, J. Woodward, B. G. Barrell, J. Parkhill, and D. A. Hopwood. 2002. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141-147.
6. Bignell, C., and C. M. Thomas. 2001. The bacterial ParA-ParB partitioning proteins. J. Biotechnol. 91:1-34.
7. Buttner, M. J., K. F. Chater, and M. J. Bibb. 1990. Cloning, disruption, and transcriptional analysis of three RNA polymerase sigma factor genes of Streptomyces coelicolor A3(2). J. Bacteriol. 172:3367-3378.
8. Chater, K. F. 1972. A morphological and genetic mapping study of white colony mutants of Streptomyces coelicolor. J. Gen. Microbiol. 72:9-28.
9. Chater, K. F. 1993. Genetics of differentiation in Streptomyces. Annu. Rev. Microbiol. 47:685-713.
10. Chater, K. F. 1998. Taking a genetic scalpel to the Streptomyces colony. Microbiology 144:1465-1478.
11. Chater, K. F. 2001. Regulation of sporulation in Streptomyces coelicolor A3(2): a checkpoint multiplex? Curr. Opin. Microbiol. 4:667-673.
12. Chater, K. F., C. J. Bruton, K. A. Plaskitt, M. J. Buttner, C. Mendez, and J. D. Helmann. 1989. The developmental fate of S. coelicolor hyphae depends upon a gene product homologous with the motility sigma factor of B. subtilis. Cell 59:133-143.
13. Davis, N. K., and K. F. Chater. 1992. The Streptomyces coelicolor whiB gene encodes a small transcription factor-like protein dispensable for growth but essential for sporulation. Mol. Gen. Genet. 232:351-358.
14. Flardh, K. 2003. Growth polarity and cell division in Streptomyces. Curr. Opin. Microbiol. 6:564-571.
15. Flardh, K., K. C. Findlay, and K. F. Chater. 1999. Association of early sporulation genes with suggested developmental decision points in Streptomyces coelicolor A3(2). Microbiology 145:2229-2243.
16. Flardh, K., E. Leibovitz, M. J. Buttner, and K. F. Chater. 2000. Generation of a non-sporulating strain of Streptomyces coelicolor A3(2) by the manipulation of a developmentally controlled ftsZ promoter. Mol. Microbiol. 38:737-749.
17. Gerdes, K., J. Moller-Jensen, and R. Bugge Jensen. 2000. Plasmid and chromosome partitioning: surprises from phylogeny. Mol. Microbiol. 37:455-466.
18. Gerdes, K., J. Moller-Jensen, G. Ebersbach, T. Kruse, and K. Nordstrom. 2004. Bacterial mitotic machineries. Cell 116:359-366.
19. Glaser, P., M. E. Sharpe, B. Raether, M. Perego, K. Ohlsen, and J. Errington. 1997. Dynamic, mitotic-like behavior of a bacterial protein required for accurate chromosome partitioning. Genes Dev. 11:1160-1168.
20. Gust, B., G. L. Challis, K. Fowler, T. Kieser, and K. F. Chater. 2003. PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc. Natl. Acad. Sci. USA 100:1541-1546.
21. Hopwood, D. A., K. F. Chater, and M. J. Bibb. 1995. Genetics of antibiotic production in Streptomyces coelicolor A3(2), a model streptomycete. Biotechnology 28:65-102.
22. Ireton, K., N. W. Gunther, and A. D. Grossman. 1994. spo0J is required for normal chromosome segregation as well as the initiation of sporulation in Bacillus subtilis. J. Bacteriol. 176:5320-5329.
23. Jakimowicz, D., K. Chater, and J. Zakrzewska-Czerwinska. 2002. The ParB protein of Streptomyces coelicolor A3(2) recognizes a cluster of parS sequences within the origin-proximal region of the linear chromosome. Mol. Microbiol. 45:1365-1377.
24. Jakimowicz, D., B. Gust, J. Zakrzewska-Czerwinska, and K. F. Chater. 2005. Developmental-stage-specific assembly of ParB complexes in Streptomyces coelicolor hyphae. J. Bacteriol. 187:3572-3580.
25. Jakimowicz, P., M. R. Cheesman, W. R. Bishai, K. F. Chater, A. J. Thomson, and M. J. Buttner. 2005. Evidence that the Streptomyces developmental protein WhiD, a member of the WhiB family, binds a [4Fe-4S] cluster. J. Biol. Chem. 280:8309-8315.
26. Kelemen, G. H., G. L. Brown, J. Kormanec, L. Potuckova, K. F. Chater, and M. J. Buttner. 1996. The positions of the sigma-factor genes, whiG and sigF, in the hierarchy controlling the development of spore chains in the aerial hyphae of Streptomyces coelicolor A3(2). Mol. Microbiol. 21:593-603.
27. Kelemen, G. H., P. H. Viollier, J. Tenor, L. Marri, M. J. Buttner, and C. J, Thompson. 2001. A connection between stress and development in the multicellular prokaryote Streptomyces coelicolor A3(2). Mol. Microbiol. 40:804-814.
28. Kieser, T., M. J. Bibb, M. J. Buttner, K. F. Chater, and D. A. Hopwood. 2000. Practical Streptomyces genetics. The John Innes Foundation, Norwich, Conn.
29. Kim, H. J., M. J. Calcutt, F. J. Schmidt, and K. F. Chater. 2000. Partitioning of the linear chromosome during sporulation of Streptomyces coelicolor A3(2) involves an oriC-linked parAB locus. J. Bacteriol. 182:1313-1320.
30. Leonard, T. A., J. Moller-Jensen, and J. Lowe. 2005. Towards understanding the molecular basis of bacterial DNA segregation. Philos. Trans. R. Soc. Lond. B 360:523-535.
31. Lewis, P. J., and J. Errington. 1997. Direct evidence for active segregation of oriC regions of the Bacillus subtilis chromosome and co-localization with the SpoOJ partitioning protein. Mol. Microbiol. 25:945-954.
32. Lewis, R. A., C. R. Bignell, W. Zeng, A. C. Jones, and C. M. Thomas. 2002. Chromosome loss from par mutants of Pseudomonas putida depends on growth medium and phase of growth. Microbiology 148:537-548.
33. Lin, D. C., and A. D. Grossman. 1998. Identification and characterization of a bacterial chromosome partitioning site. Cell 92:675-685.
34. Lin, D. C., P. A. Levin, and A. D. Grossman. 1997. Bipolar localization of a chromosome partition protein in Bacillus subtilis. Proc. Natl. Acad. Sci. USA 94:4721-4726.
35. Marston, A. L., and J. Errington. 1999. Dynamic movement of the ParA-like Soj protein of B. subtilis and its dual role in nucleoid organization and developmental regulation. Mol. Cell 4:673-682.
36. McCormick, J. R., E. P. Su, A. Driks, and R. Losick. 1994. Growth and viability of Streptomyces coelicolor mutant for the cell division gene ftsZ. Mol. Microbiol. 14:243-254.
37. Mohl, D. A., J. Easter, Jr., and J. W. Gober. 2001. The chromosome partitioning protein, ParB, is required for cytokinesis in Caulobacter crescentus. Mol. Microbiol. 42:741-755.
38. Mohl, D. A., and J. W. Gober. 1997. Cell cycle-dependent polar localization of chromosome partitioning proteins in Caulobacter crescentus. Cell 88:675-684.
39. Ogasawara, N., and H. Yoshikawa. 1992. Genes and their organization in the replication origin region of the bacterial chromosome. Mol. Microbiol. 6:629-634.
40. Omura, S., H. Ikeda, J. Ishikawa, A. Hanamoto, C. Takahashi, M. Shinose, Y. Takahashi, H. Horikawa, H. Nakazawa, T. Osonoe, H. Kikuchi, T. Shiba, Y. Sakaki, and M. Hattori. 2001. Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. Proc. Natl. Acad. Sci. USA 98:12215-12220.
41. E is required for normal cell wall structure in Streptomyces coelicolor A3(2). J. Bacteriol. 181:204-211.
42. Pogliano, K., J. Pogliano, and E. Becker. 2003. Chromosome segregation in Eubacteria. Curr. Opin. Microbiol. 6:586-593.
43. Potuckova, L., G. H. Kelemen, K. C. Findlay, M. A. Lonetto, M. J. Buttner, and J. Kormanec. 1995. A new RNA polymerase sigma factor, sigma F, is required for the late stages of morphological differentiation in Streptomyces spp. Mol. Microbiol. 17:37-48.
44. Ryding, N. J., G. H. Kelemen, C. A. Whatling, K. Flardh, M. J. Buttner, and K. F. Chater. 1998. A developmentally regulated gene encoding a repressor-like protein is essential for sporulation in Streptomyces coelicolor A3(2). Mol. Microbiol. 29:343-357.
45. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
46. Schwedock, J., J. R. McCormick, E. R. Angert, J. R. Nodwell, and R. Losick. 1997. Assembly of the cell division protein FtsZ into ladder-like structures in the aerial hyphae of Streptomyces coelicolor. Mol. Microbiol. 25:847-858.
47. Sharpe, M. E., and J. Errington. 1996. The Bacillus subtilis soj-spo0J locus is required for a centromere-like function involved in prespore chromosome partitioning. Mol. Microbiol. 21:501-509.
48. Sherratt, D. J. 2003. Bacterial chromosome dynamics. Science 301:780-785.
49. Soliveri, J., K. L. Brown, M. J. Buttner, and K. F. Chater. 1992. Two promoters for the whiB sporulation gene of Streptomyces coelicolor A3(2) and their activities in relation to development. J. Bacteriol. 174:6215-6220.
50. Sun, J., G. H. Kelemen, J. M. Fernandez-Abalos, and M. J. Bibb. 1999. Green fluorescent protein as a reporter for spatial and temporal gene expression in Streptomyces coelicolor A3(2). Microbiology 145:2221-2227.
51. Webb, C. D., A. Teleman, S. Gordon, A. Straight, A. Belmont, D. C. Lin, A. D. Grossman, A. Wright, and R. Losick. 1997. Bipolar localization of the replication origin regions of chromosomes in vegetative and sporulating cells of B. subtilis. Cell 88:667-674.
52. Wu, L. J. 2004. Structure and segregation of the bacterial nucleoid. Curr. Opin. Genet. Dev. 14:126-132.